Crosslinking of Translation Factor EF-G to Proteins of the Bacterial Ribosome Before and After Translocation

Journal of Molecular Biology

Volumn 368, Issue 5, 2007, Pages 1412-1425

  Nechifor, Roxana ^a   Wilson, Kevin S ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

bacterial ribosome; chemical crosslinking; elongation factor; ribosomal protein

Indexed keywords

AMINO ACID; BACTERIAL PROTEIN; ELONGATION FACTOR G; MESSENGER RNA; RIBOSOME PROTEIN; TRANSFER RNA;

ARTICLE; BACTERIAL TRANSLOCATION; CATALYSIS; CROSS LINKING; IMMUNOBLOTTING; LIPID HYDROLYSIS; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN LOCALIZATION; RIBOSOME;

BACTERIA (MICROORGANISMS);

EID: 34247205376     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.03.009     Document Type: Article

References (50)

1. Berchtold H., Reshetnikova L., Reiser C.O., Schirmer N.K., Sprinzl M., and Hilgenfeld R. Crystal structure of active elongation factor Tu reveals major domain rearrangements. Nature 365 (1993) 126-132
2. Czworkowski J., Wang J., Steitz T.A., and Moore P.B. The crystal structure of elongation factor G complexed with GDP, at 2.7 Å resolution. EMBO J. 13 (1994) 3661-3668
3. Ævarsson A., Brazhnikov E., Garber M., Zheltonosova J., Chirgadze Y., al-Karadaghi S., et al. Three-dimensional structure of the ribosomal translocase: elongation factor G from Thermus thermophilus. EMBO J. 13 (1994) 3669-3677
4. Nissen P., Kjeldgaard M., Thirup S., Polekhina G., Reshetnikova L., Clark B.F., and Nyborg J. Crystal structure of the ternary complex of Phe-tRNAPhe, EF-Tu, and a GTP analog. Science 270 (1995) 1464-1472
5. Bodley J.W., and Lin L. Interaction of E. coli G factor with the 50S ribosomal subunit. Nature 227 (1970) 60-61
6. Wilson K.S., and Noller H.F. Mapping the position of translational elongation factor EF-G in the ribosome by directed hydroxyl radical probing. Cell 92 (1998) 131-139
7. Agrawal R.K., Penczek P., Grassucci R.A., and Frank J. Visualization of elongation factor G on the Escherichia coli 70S ribosome: the mechanism of translocation. Proc. Natl Acad. Sci. USA 95 (1998) 6134-6138
8. Savelsbergh A., Matassova N.B., Rodnina M.V., and Wintermeyer W. Role of domains 4 and 5 in elongation factor G functions on the ribosome. J. Mol. Biol. 300 (2000) 951-961
9. Martemyanov K.A., and Gudkov A.T. Domain III of elongation factor G from Thermus thermophilus is essential for induction of GTP hydrolysis on the ribosome. J. Biol. Chem. 275 (2000) 35820-35824
10. Stark H., Rodnina M.V., Rinke-Appel J., Brimacombe R., Wintermeyer W., and van Heel M. Visualization of elongation factor Tu on the Escherichia coli ribosome. Nature 389 (1997) 403-406
11. Stark H., Rodnina M.V., Wieden H.J., van Heel M., and Wintermeyer W. Large-scale movement of elongation factor G and extensive conformational change of the ribosome during translocation. Cell 100 (2000) 301-309
12. Valle M., Zavialov A., Sengupta J., Rawat U., Ehrenberg M., and Frank J. Locking and unlocking of ribosomal motions. Cell 114 (2003) 123-134
13. Valle M., Zavialov A., Li W., Stagg S.M., Sengupta J., Nielsen R.C., et al. Incorporation of aminoacyl-tRNA into the ribosome as seen by cryo-electron microscopy. Nature Struct. Biol. 10 (2003) 899-906
14. Maassen J.A., and Möller W. Identification by photo-affinity labeling of the proteins in Escherichia coli ribosomes involved in elongation factor G-dependent GDP binding. Proc. Natl Acad. Sci. USA 71 (1974) 1277-1280
15. San Jose C., Kurland C.G., and Stoffler G. The protein neighborhood of ribosome-bound elongation factor Tu. FEBS LettERS 72 (1976) 133-137
16. Maassen J.A., and Möller W. Elongation factor G-dependent binding of a photoreactive GTP analogue to Escherichia coli ribosomes results in labeling of protein L11. J. Biol. Chem. 253 (1978) 2777-2783
17. Girshovich A.S., Kurtskhalia T.V., Ovchinnikov Yu A., and Vasiliev V.D. Localization of the elongation factor G on Escherichia coli ribosome. FEBS LettERS 130 (1981) 54-59
18. Maassen J.A., and Möller W. Photochemical cross-linking of elongation factor G to 70-S ribosomes from Escherichia coli by 4-(6-formyl-3-azidophenoxy)butyrimidate. Eur. J. Biochem. 115 (1981) 279-285
19. Sköld S.E. Chemical cross-linking of elongation factor G to both subunits of the 70-S ribosomes from Escherichia coli. Eur. J. Biochem. 127 (1982) 225-229
20. Nag B., Johnson A.E., and Traut R.R. Identification of the elongation factor Tu binding site on 70S E. coli ribosomes by chemical crosslinking. Indian J. Biochem. Biophys. 32 (1995) 343-350
21. Mohr D., Wintermeyer W., and Rodnina M.V. GTPase activation of elongation factors Tu and G on the ribosome. Biochemistry 41 (2002) 12520-12528
22. Diaconu M., Kothe U., Schlunzen F., Fischer N., Harms J.M., Tonevitsky A.G., et al. Structural basis for the function of the ribosomal L7/12 stalk in factor binding and GTPase activation. Cell 121 (2005) 991-1004
23. Kirsebom L.A., Amons R., and Isaksson L.A. Primary structures of mutationally altered ribosomal protein L7/L12 and their effects on cellular growth and translational accuracy. Eur. J. Biochem. 156 (1986) 669-675
24. Bilgin N., Claesens F., Pahverk H., and Ehrenberg M. Kinetic properties of Escherichia coli ribosomes with altered forms of S12. J. Mol. Biol. 224 (1992) 1011-1027
25. Gavrilova L.P., Koteliansky V.E., and Spirin A.S. Ribosomal protein S12 and 'non-enzymatic' translocation. FEBS LettERS 45 (1974) 324-328
26. Cukras A.R., Southworth D.R., Brunelle J.L., Culver G.M., and Green R. Ribosomal proteins S12 and S13 function as control elements for translocation of the mRNA:tRNA complex. Mol. Cell 12 (2003) 321-328
27. Sinz A. Chemical cross-linking and mass spectrometry to map three-dimensional protein structures and protein-protein interactions. Mass Spectrom. Rev. 25 (2006) 663-682
28. Wilson K.S., and Nechifor R. Interactions of translation factor EF-G with the bacterial ribosome before and after mRNA translocation. J. Mol. Biol. 337 (2004) 15-30
29. Stöffler G., and Wittmann H.G. Ribosomal proteins. XXV. Immunological studies on Escherichia coli ribosomal proteins. J. Mol. Biol. 62 (1971) 407-409
30. Ofengand J., Denman R., Nurse K., Liebman A., Malarek D., Focella A., and Zenchoff G. Affinity labeling of tRNA-binding sites on ribosomes. Methods Enzymol. 164 (1988) 372-397
31. Wower J., Hixson S.S., and Zimmermann R.A. Labeling the peptidyltransferase center of the Escherichia coli ribosome with photoreactive tRNA(Phe) derivatives containing azidoadenosine at the 3′ end of the acceptor arm: a model of the tRNA-ribosome complex. Proc. Natl Acad. Sci. USA 86 (1989) 5232-5236
32. Wower J., Kirillov S.V., Wower I.K., Guven S., Hixson S.S., and Zimmermann R.A. Transit of tRNA through the Escherichia coli ribosome. Cross-linking of the 3′ end of tRNA to specific nucleotides of the 23 S ribosomal RNA at the A, P, and E sites. J. Biol. Chem. 275 (2000) 37887-37894
33. Savelsbergh A., Katunin V.I., Mohr D., Peske F., Rodnina M.V., and Wintermeyer W. An elongation factor G-induced ribosome rearrangement precedes tRNA-mRNA translocation. Mol. Cell 11 (2003) 1517-1523
34. Frank J., and Agrawal R.K. A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406 (2000) 318-322
35. Laurberg M., Kristensen O., Martemyanov K., Gudkov A.T., Nagaev I., Hughes D., and Liljas A. Structure of a mutant EF-G reveals domain III and possibly the fusidic acid binding site. J. Mol. Biol. 303 (2000) 593-603
36. Bodley J.W., Zieve F.J., and Lin L. Studies on translocation. IV. The hydrolysis of a single round of guanosine triphosphate in the presence of fusidic acid. J. Biol. Chem. 245 (1970) 5662-5667
37. Johanson U., Aevarsson A., Liljas A., and Hughes D. The dynamic structure of EF-G studied by fusidic acid resistance and internal revertants. J. Mol. Biol. 258 (1996) 420-432
38. Shimmin L.C., Ramirez C., Matheson A.T., and Dennis P.P. Sequence alignment and evolutionary comparison of the L10 equivalent and L12 equivalent ribosomal proteins from archaebacteria, eubacteria, and eucaryotes. J. Mol. Evol. 29 (1989) 448-462
39. Gao H., Sengupta J., Valle M., Korostelev A., Eswar N., Stagg S.M., et al. Study of the structural dynamics of the E. coli 70S ribosome using real-space refinement. Cell 113 (2003) 789-801
40. Agrawal R.K., Linde J., Sengupta J., Nierhaus K.H., and Frank J. Localization of L11 protein on the ribosome and elucidation of its involvement in EF-G-dependent translocation. J. Mol. Biol. 311 (2001) 777-787
41. Datta P.P., Sharma M.R., Qi L., Frank J., and Agrawal R.K. Interaction of the G′ domain of elongation factor G and the C-terminal domain of ribosomal protein L7/L12 during translocation as revealed by cryo-EM. Mol. Cell 20 (2005) 723-731
42. Kothe U., Wieden H.J., Mohr D., and Rodnina M.V. Interaction of helix D of elongation factor Tu with helices 4 and 5 of protein L7/12 on the ribosome. J. Mol. Biol. 336 (2004) 1011-1021
43. Buckel P., Buchberger A., Bock A., and Wittmann H.G. Alteration of ribosomal protein L6 in mutants of Escherichia coli resistant to gentamicin. Mol. Gen. Genet. 158 (1977) 47-54
44. Davies C., Bussiere D.E., Golden B.L., Porter S.J., Ramakrishnan V., and White S.W. Ribosomal proteins S5 and L6: high-resolution crystal structures and roles in protein synthesis and antibiotic resistance. J. Mol. Biol. 279 (1998) 873-888
45. Vicens Q., and Westhof E. Crystal structure of geneticin bound to a bacterial 16S ribosomal RNA A site oligonucleotide. J. Mol. Biol. 326 (2003) 1175-1188
46. Cabañas M.J., Vazquez D., and Modolell J. Inhibition of ribosomal translocation by aminoglycoside antibiotics. Biochem. Biophys. Res. Commun. 83 (1978) 991-997
47. Christodoulou J., Larsson G., Fucini P., Connell S.R., Pertinhez T.A., Hanson C.L., et al. Heteronuclear NMR investigations of dynamic regions of intact Escherichia coli ribosomes. Proc. Natl Acad. Sci. USA 101 (2004) 10949-10954
48. Hamman B.D., Oleinikov A.V., Jokhadze G.G., Traut R.R., and Jameson D.M. Rotational and conformational dynamics of Escherichia coli ribosomal protein L7/L12. Biochemistry 35 (1996) 16672-16679
49. Helgstrand M., Mandava C.S., Mulder F.A., Liljas A., Sanyal S., and Akke M. The ribosomal stalk binds to translation factors IF2, EF-Tu, EF-G and RF3 via a conserved region of the L12 C-terminal domain. J. Mol. Biol. 365 (2007) 468-479
50. Selmer M., Dunham C.M., Murphy F.V., Weixlbaumer A., Petry S., Kelley A.C., et al. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313 (2006) 1935-1942